[en] Among the large matrix metalloproteinases (MMPs) family, MMP-12, also referred to as macrophage elastase, plays a significant role in chronic pulmonary pathologies characterized by an intense tissue remodeling such as asthma and COPD. This review will summarize knowledge about MMP-12 structure, functions and mechanisms of activation and regulation, including potential MMP-12 modulation by microRNA. As MMP-12 is involved in many tissue remodeling diseases, efforts have been made to develop specific synthetic inhibitors. However, at this time, very few chemical inhibitors have proved to be efficient and specific to a particular MMP. The relevance of silencing MMP-12 by RNA interference is highlighted. The specificity of this approach using siRNA or shRNA and the strategies to deliver these molecules in the lung are discussed.
Disciplines :
Human health sciences: Multidisciplinary, general & others
Author, co-author :
Garbacki, Nancy ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Protéines et glycoprot. de matr.extracell. et membran.basal.
Piette, Jacques ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Virologie - Immunologie - GIGA-Research
Cataldo, Didier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Crahay, Céline
Colige, Alain ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Protéines et glycoprot. de matr.extracell. et membran.basal.
Language :
English
Title :
Matrix metalloproteinase 12 silencing: A therapeutic approach to treat pathological lung tissue remodeling?
Birkedal-Hansen H., Moore W.G., Bodden M.K., Windsor L.J., Birkedal-Hansen B., DeCarlo A., et al. Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 4 (1993) 197-250
Fu X., Parks W.C., and Heinecke J.W. Activation and silencing of matrix metalloproteinases. Semin Cell Dev Biol 19 (2008) 2-13
Wu L., Fan J., Matsumoto S., and Watanabe T. Induction and regulation of matrix metalloproteinase-12 by cytokines and CD40 signaling in monocyte/macrophages. Biochem Biophys Res Commun 269 (2000) 808-815
Lavigne M.C., Thakker P., Gunn J., Wong A., Miyashiro J.S., Wasserman A.M., et al. Human bronchial epithelial cells express and secrete MMP-12. Biochem Biophys Res Commun 324 (2004) 534-546
Lian X., Qin Y., Hossain S.A., Yang L., White A., Xu H., et al. Overexpression of Stat3C in pulmonary epithelium protects against hyperoxic lung injury. J Immunol 174 (2005) 7250-7256
Xie S., Issa R., Sukkar M.B., Oltmanns U., Bhavsar P.K., Papi A., et al. Induction and regulation of matrix metalloproteinase-12 in human airway smooth muscle cells. Respir Res 6 (2005) 148
Lagente V., and Boichot E. Models for chronic obstructive pulmonary disease involving matrix metalloproteinases. Drug Discov Today Dis Models 3 (2006) 231-236
Nenan S., Planquois J.M., Berna P., De Mendez I., Hitier S., Shapiro S.D., et al. Analysis of the inflammatory response induced by rhMMP-12 catalytic domain instilled in mouse airways. Int Immunopharmacol 5 (2005) 511-524
Starcher B.C. Elastin and the lung. Thorax 41 (1986) 577-585
Belvisi M.G., and Bottomley K.M. The role of matrix metalloproteinases (MMPs) in the pathophysiology of chronic obstructive pulmonary disease (COPD): a therapeutic role for inhibitors of MMPs?. Inflamm Res 52 (2003) 95-100
Demedts I.K., Morel-Montero A., Lebecque S., Pacheco Y., Cataldo D., Joos G.F., et al. Elevated MMP-12 protein levels in induced sputum from patients with COPD. Thorax 61 (2006) 196-201
Shapiro S.D. Proteinases in chronic obstructive pulmonary disease. Biochem Soc Trans 30 (2002) 98-102
Babusyte A., Stravinskaite K., Jeroch J., Lotvall J., Sakalauskas R., and Sitkauskiene B. Patterns of airway inflammation and MMP-12 expression in smokers and ex-smokers with COPD. Respir Res 8 (2007) 81
Hogg J.C., Chu F., Utokaparch S., Woods R., Elliott W.M., Buzatu L., et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 350 (2004) 2645-2653
Shapiro S.D. Elastolytic metalloproteinases produced by human mononuclear phagocytes. Potential roles in destructive lung disease. Am J Respir Crit Care Med 150 (1994) S160-S164
Lavigne M.C., and Eppihimer M.J. Cigarette smoke condensate induces MMP-12 gene expression in airway-like epithelia. Biochem Biophys Res Commun 330 (2005) 194-203
Hautamaki R.D., Kobayashi D.K., Senior R.M., and Shapiro S.D. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277 (1997) 2002-2004
Maes T., Bracke K.R., Vermaelen K.Y., Demedts I.K., Joos G.F., Pauwels R.A., et al. Murine TLR4 is implicated in cigarette smoke-induced pulmonary inflammation. Int Arch Allergy Immunol 141 (2006) 354-368
Molet S., Belleguic C., Lena H., Germain N., Bertrand C.P., Shapiro S.D., et al. Increase in macrophage elastase (MMP-12) in lungs from patients with chronic obstructive pulmonary disease. Inflamm Res 54 (2005) 31-36
Pascual R.M., and Peters S.P. Airway remodeling contributes to the progressive loss of lung function in asthma: an overview. J Allergy Clin Immunol 116 (2005) 477-486 [quiz 487]
Beasley R., Page C., and Lichtenstein L. Airway remodelling in asthma. Clin Exp Allergy Rev 2 (2002) 109-116
Sarpong S.B., Zhang L.Y., and Kleeberger S.R. A novel mouse model of experimental asthma. Int Arch Allergy Immunol 132 (2003) 346-354
Pouladi M.A., Robbins C.S., Swirski F.K., Cundall M., McKenzie A.N., Jordana M., et al. Interleukin-13-dependent expression of matrix metalloproteinase-12 is required for the development of airway eosinophilia in mice. Am J Respir Cell Mol Biol 30 (2004) 84-90
Chiba Y., Yu Y., Sakai H., and Misawa M. Increase in the expression of matrix metalloproteinase-12 in the airways of rats with allergic bronchial asthma. Biol Pharm Bull 30 (2007) 318-323
Di Valentin E., Crahay C., Garbacki N., Hennuy B., Guéders M., Noël A., et al. New asthma biomarkers: lessons from murine models of acute and chronic asthma. Am J Physiol Lung Cell Mol Physiol 296 (2009) L185-L197
Amrani Y., and Panettieri Jr. R.A. Cytokines induce airway smooth muscle cell hyperresponsiveness to contractile agonists. Thorax 53 (1998) 713-716
Cataldo D.D., Tournoy K.G., Vermaelen K., Munaut C., Foidart J.M., Louis R., et al. Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation. Am J Pathol 161 (2002) 491-498
Warner R.L., Lukacs N.W., Shapiro S.D., Bhagarvathula N., Nerusu K.C., Varani J., et al. Role of metalloelastase in a model of allergic lung responses induced by cockroach allergen. Am J Pathol 165 (2004) 1921-1930
Lagente V., Manoury B., Nenan S., Le Quement C., Martin-Chouly C., and Boichot E. Role of matrix metalloproteinases in the development of airway inflammation and remodeling. Braz J Med Biol Res 38 (2005) 1521-1530
Shapiro S.D., Griffin G.L., Gilbert D.J., Jenkins N.A., Copeland N.G., Welgus H.G., et al. Molecular cloning, chromosomal localization, and bacterial expression of a murine macrophage metalloelastase. J Biol Chem 267 (1992) 4664-4671
Shapiro S.D., Kobayashi D.K., and Ley T.J. Cloning and characterization of a unique elastolytic metalloproteinase produced by human alveolar macrophages. J Biol Chem 268 (1993) 23824-23829
Fu J.Y., Lyga A., Shi H., Blue M.L., Dixon B., and Chen D. Cloning, expression, purification, and characterization of rat MMP-12. Protein Expr Purif 21 (2001) 268-274
Chen Y.E. MMP-12, an old enzyme plays a new role in the pathogenesis of rheumatoid arthritis?. Am J Pathol 165 (2004) 1069-1070
Bertini I., Calderone V., Fragai M., Luchinat C., Mangani S., and Terni B. X-ray structures of binary and ternary enzyme-product-inhibitor complexes of matrix metalloproteinases. Angew Chem Int Ed Engl 42 (2003) 2673-2676
Kerkela E., Bohling T., Herva R., Uria J.A., and Saarialho-Kere U. Human macrophage metalloelastase (MMP-12) expression is induced in chondrocytes during fetal development and malignant transformation. Bone 29 (2001) 487-493
Gronski Jr. T.J., Martin R.L., Kobayashi D.K., Walsh B.C., Holman M.C., Huber M., et al. Hydrolysis of a broad spectrum of extracellular matrix proteins by human macrophage elastase. J Biol Chem 272 (1997) 12189-12194
Ashworth J.L., Murphy G., Rock M.J., Sherratt M.J., Shapiro S.D., Shuttleworth C.A., et al. Fibrillin degradation by matrix metalloproteinases: implications for connective tissue remodelling. Biochem J 340 Pt 1 (1999) 171-181
Matsumoto S., Kobayashi T., Katoh M., Saito S., Ikeda Y., Kobori M., et al. Expression and localization of matrix metalloproteinase-12 in the aorta of cholesterol-fed rabbits: relationship to lesion development. Am J Pathol 153 (1998) 109-119
Shipley J.M., Wesselschmidt R.L., Kobayashi D.K., Ley T.J., and Shapiro S.D. Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci U S A 93 (1996) 3942-3946
Houghton A.M., Quintero P.A., Perkins D.L., Kobayashi D.K., Kelley D.G., Marconcini L.A., et al. Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest 116 (2006) 753-759
Chandler S., Cossins J., Lury J., and Wells G. Macrophage metalloelastase degrades matrix and myelin proteins and processes a tumour necrosis factor-alpha fusion protein. Biochem Biophys Res Commun 228 (1996) 421-429
Belaaouaj A.A., Li A., Wun T.C., Welgus H.G., and Shapiro S.D. Matrix metalloproteinases cleave tissue factor pathway inhibitor. Effects on coagulation. J Biol Chem 275 (2000) 27123-27128
Dong Z., Kumar R., Yang X., and Fidler I.J. Macrophage-derived metalloelastase is responsible for the generation of angiostatin in Lewis lung carcinoma. Cell 88 (1997) 801-810
Cornelius L.A., Nehring L.C., Harding E., Bolanowski M., Welgus H.G., Kobayashi D.K., et al. Matrix metalloproteinases generate angiostatin: effects on neovascularization. J Immunol 161 (1998) 6845-6852
Dwivedi A., and George S. MMP-12 is important for VSMC proliferation and migration: role of B-catenin signalling. Vascul Pharmacol 45 (2006) e129
Huang H., and He X. Wnt/beta-catenin signaling: new (and old) players and new insights. Curr Opin Cell Biol 20 (2008) 119-125
Curci J.A., Liao S., Huffman M.D., Shapiro S.D., and Thompson R.W. Expression and localization of macrophage elastase (matrix metalloproteinase-12) in abdominal aortic aneurysms. J Clin Invest 102 (1998) 1900-1910
Wu L., Tanimoto A., Murata Y., Fan J., Sasaguri Y., and Watanabe T. Induction of human matrix metalloproteinase-12 gene transcriptional activity by GM-CSF requires the AP-1 binding site in human U937 monocytic cells. Biochem Biophys Res Commun 285 (2001) 300-307
Clark I.M., Swingler T.E., Sampieri C.L., and Edwards D.R. The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 40 (2008) 1362-1378
Feinberg M.W., Jain M.K., Werner F., Sibinga N.E., Wiesel P., Wang H., et al. Transforming growth factor-beta 1 inhibits cytokine-mediated induction of human metalloelastase in macrophages. J Biol Chem 275 (2000) 25766-25773
Rosen R.L., Winestock K.D., Chen G., Liu X., Hennighausen L., and Finbloom D.S. Granulocyte-macrophage colony-stimulating factor preferentially activates the 94-kD STAT5A and an 80-kD STAT5A isoform in human peripheral blood monocytes. Blood 88 (1996) 1206-1214
Lappalainen U., Whitsett J.A., Wert S.E., Tichelaar J.W., and Bry K. Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. Am J Respir Cell Mol Biol 32 (2005) 311-318
Hoffmann E., Ashouri J., Wolter S., Doerrie A., Dittrich-Breiholz O., Schneider H., et al. Transcriptional regulation of EGR-1 by the interleukin-1-JNK-MKK7-c-Jun pathway. J Biol Chem 283 (2008) 12120-12128
Elias J.A., Kang M.J., Crothers K., Homer R., and Lee C.G. State of the art. Mechanistic heterogeneity in chronic obstructive pulmonary disease: insights from transgenic mice. Proc Am Thorac Soc 3 (2006) 494-498
Greenlee K.J., Werb Z., and Kheradmand F. Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol Rev 87 (2007) 69-98
Lanone S., Zheng T., Zhu Z., Liu W., Lee C.G., Ma B., et al. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J Clin Invest 110 (2002) 463-474
Fichtner-Feigl S., Strober W., Kawakami K., Puri R.K., and Kitani A. IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med 12 (2006) 99-106
Wang X., Inoue S., Gu J., Miyoshi E., Noda K., Li W., et al. Dysregulation of TGF-beta1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice. Proc Natl Acad Sci U S A 102 (2005) 15791-15796
Horton M.R., Shapiro S., Bao C., Lowenstein C.J., and Noble P.W. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J Immunol 162 (1999) 4171-4176
Ito S., Kimura K., Haneda M., Ishida Y., Sawada M., and Isobe K. Induction of matrix metalloproteinases (MMP3, MMP12 and MMP13) expression in the microglia by amyloid-beta stimulation via the PI3K/Akt pathway. Exp Gerontol 42 (2007) 532-537
Xu J., Xu F., and Barrett E. Metalloelastase in lungs and alveolar macrophages is modulated by extracellular substance P in mice. Am J Physiol Lung Cell Mol Physiol 295 (2008) L162-L170
Bracke K., Cataldo D., Maes T., Gueders M., Noel A., Foidart J.M., et al. Matrix metalloproteinase-12 and cathepsin D expression in pulmonary macrophages and dendritic cells of cigarette smoke-exposed mice. Int Arch Allergy Immunol 138 (2005) 169-179
Arikan M.C., Shapiro S.D., and Mariani T.J. Induction of macrophage elastase (MMP-12) gene expression by statins. J Cell Physiol 204 (2005) 139-145
miRBase. .
van Rooij E., Sutherland L.B., Thatcher J.E., DiMaio J.M., Naseem R.H., Marshall W.S., et al. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 105 (2008) 13027-13032
Sengupta S., den Boon J.A., Chen I.H., Newton M.A., Stanhope S.A., Cheng Y.J., et al. MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci U S A 105 (2008) 5874-5878
Raza S.L., Nehring L.C., Shapiro S.D., and Cornelius L.A. Proteinase-activated receptor-1 regulation of macrophage elastase (MMP-12) secretion by serine proteinases. J Biol Chem 275 (2000) 41243-41250
Churg A., Wang X., Wang R.D., Meixner S.C., Pryzdial E.L., and Wright J.L. Alpha1-antitrypsin suppresses TNF-alpha and MMP-12 production by cigarette smoke-stimulated macrophages. Am J Respir Cell Mol Biol 37 (2007) 144-151
Lijnen H.R. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost 86 (2001) 324-333
Pepper M.S. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21 (2001) 1104-1117
Shukla A., Barrett T.F., Nakayama K.I., Nakayama K., Mossman B.T., and Lounsbury K.M. Transcriptional up-regulation of MMP12 and MMP13 by asbestos occurs via a PKCdelta-dependent pathway in murine lung. FASEB J 20 (2006) 997-999
Grumelli S., Corry D.B., Song L.Z., Song L., Green L., Huh J., et al. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med 1 (2004) e8
He C.S., Wilhelm S.M., Pentland A.P., Marmer B.L., Grant G.A., Eisen A.Z., et al. Tissue cooperation in a proteolytic cascade activating human interstitial collagenase. Proc Natl Acad Sci U S A 86 (1989) 2632-2636
Carmeliet P., Moons L., Lijnen R., Baes M., Lemaitre V., Tipping P., et al. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat Genet 17 (1997) 439-444
Gossas T., and Danielson U.H. Characterization of Ca2+ interactions with matrix metallopeptidase-12: implications for matrix metallopeptidase regulation. Biochem J 398 (2006) 393-398
Gill S.E., and Parks W.C. Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 40 (2008) 1334-1347
Kassim S.Y., Fu X., Liles W.C., Shapiro S.D., Parks W.C., and Heinecke J.W. NADPH oxidase restrains the matrix metalloproteinase activity of macrophages. J Biol Chem 280 (2005) 30201-30205
Vaalamo M., Kariniemi A.L., Shapiro S.D., and Saarialho-Kere U. Enhanced expression of human metalloelastase (MMP-12) in cutaneous granulomas and macrophage migration. J Invest Dermatol 112 (1999) 499-505
Saarialho-Kere U., Kerkela E., Jeskanen L., Hasan T., Pierce R., Starcher B., et al. Accumulation of matrilysin (MMP-7) and macrophage metalloelastase (MMP-12) in actinic damage. J Invest Dermatol 113 (1999) 664-672
Suomela S., Kariniemi A.L., Snellman E., and Saarialho-Kere U. Metalloelastase (MMP-12) and 92-kDa gelatinase (MMP-9) as well as their inhibitors, TIMP-1 and -3, are expressed in psoriatic lesions. Exp Dermatol 10 (2001) 175-183
Johnson J.L. Matrix metalloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability. Expert Rev Cardiovasc Ther 5 (2007) 265-282
Yamada S., Wang K.Y., Tanimoto A., Fan J., Shimajiri S., Kitajima S., et al. Matrix metalloproteinase 12 accelerates the initiation of atherosclerosis and stimulates the progression of fatty streaks to fibrous plaques in transgenic rabbits. Am J Pathol 172 (2008) 1419-1429
Dong Z., Yoneda J., Kumar R., and Fidler I.J. Angiostatin-mediated suppression of cancer metastases by primary neoplasms engineered to produce granulocyte/macrophage colony-stimulating factor. J Exp Med 188 (1998) 755-763
Gorrin-Rivas M.J., Arii S., Mori A., Takeda Y., Mizumoto M., Furutani M., et al. Implications of human macrophage metalloelastase and vascular endothelial growth factor gene expression in angiogenesis of hepatocellular carcinoma. Ann Surg 231 (2000) 67-73
Yang W., Arii S., Gorrin-Rivas M.J., Mori A., Onodera H., and Imamura M. Human macrophage metalloelastase gene expression in colorectal carcinoma and its clinicopathologic significance. Cancer 91 (2001) 1277-1283
Kerkela E., Ala-Aho R., Jeskanen L., Rechardt O., Grenman R., Shapiro S.D., et al. Expression of human macrophage metalloelastase (MMP-12) by tumor cells in skin cancer. J Invest Dermatol 114 (2000) 1113-1119
Cuniasse P., Devel L., Makaritis A., Beau F., Georgiadis D., Matziari M., et al. Future challenges facing the development of specific active-site-directed synthetic inhibitors of MMPs. Biochimie 87 (2005) 393-402
Bertini I., Calderone V., Cosenza M., Fragai M., Lee Y.M., Luchinat C., et al. Conformational variability of matrix metalloproteinases: beyond a single 3D structure. Proc Natl Acad Sci U S A 102 (2005) 5334-5339
Skiles J.W., Gonnella N.C., and Jeng A.Y. The design, structure, and therapeutic application of matrix metalloproteinase inhibitors. Curr Med Chem 8 (2001) 425-474
Dive V., Georgiadis D., Matziari M., Makaritis A., Beau F., Cuniasse P., et al. Phosphinic peptides as zinc metalloproteinase inhibitors. Cell Mol Life Sci 61 (2004) 2010-2019
Hu J., Van den Steen P.E., Sang Q.X., and Opdenakker G. Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases. Nat Rev Drug Discov 6 (2007) 480-498
Devel L., Rogakos V., David A., Makaritis A., Beau F., Cuniasse P., et al. Development of selective inhibitors and substrate of matrix metalloproteinase-12. J Biol Chem 281 (2006) 11152-11160
Schiodt C.B., Buchardt J., Terp G.E., Christensen U., Brink M., Berger Larsen Y., et al. Phosphinic peptide inhibitors of macrophage metalloelastase (MMP-12). Selectivity and mechanism of binding. Curr Med Chem 8 (2001) 967-976
Le Quement C., Guenon I., Gillon J.Y., Valenca S., Cayron-Elizondo V., Lagente V., et al. The selective MMP-12 inhibitor, AS111793 reduces airway inflammation in mice exposed to cigarette smoke. Br J Pharmacol 154 (2008) 1206-1215
Ma D., Jiang Y., Chen F., Gong L.K., Ding K., Xu Y., et al. Selective inhibition of matrix metalloproteinase isozymes and in vivo protection against emphysema by substituted gamma-keto carboxylic acids. J Med Chem 49 (2006) 456-458
Mannino C., Nievo M., Machetti F., Papakyriakou A., Calderone V., Fragai M., et al. Synthesis of bicyclic molecular scaffolds (BTAa): an investigation towards new selective MMP-12 inhibitors. Bioorg Med Chem 14 (2006) 7392-7403
Dublanchet A.C., Ducrot P., Andrianjara C., O'Gara M., Morales R., Compere D., et al. Structure-based design and synthesis of novel non-zinc chelating MMP-12 inhibitors. Bioorg Med Chem Lett 15 (2005) 3787-3790
Ando N., and Terashima S. Synthesis and matrix metalloproteinase (MMP)-12 inhibitory activity of ageladine A and its analogs. Bioorg Med Chem Lett 17 (2007) 4495-4499
Fingleton B. MMPs as therapeutic targets - still a viable option?. Semin Cell Dev Biol 19 (2008) 61-68
Cataldo D.D., Gueders M.M., Rocks N., Sounni N.E., Evrard B., Bartsch P., et al. Pathogenic role of matrix metalloproteases and their inhibitors in asthma and chronic obstructive pulmonary disease and therapeutic relevance of matrix metalloproteases inhibitors. Cell Mol Biol (Noisy-le-grand) 49 (2003) 875-884
Gueders M.M., Balbin M., Rocks N., Foidart J.M., Gosset P., Louis R., et al. Matrix metalloproteinase-8 deficiency promotes granulocytic allergen-induced airway inflammation. J Immunol 175 (2005) 2589-2597
de Fougerolles A., Vornlocher H.P., Maraganore J., and Lieberman J. Interfering with disease: a progress report on siRNA-based therapeutics. Nat Rev Drug Discov 6 (2007) 443-453
Filipowicz W., Jaskiewicz L., Kolb F.A., and Pillai R.S. Post-transcriptional gene silencing by siRNAs and miRNAs. Curr Opin Struct Biol 15 (2005) 331-341
Valencia-Sanchez M.A., Liu J., Hannon G.J., and Parker R. Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20 (2006) 515-524
Chapman E.J., and Carrington J.C. Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8 (2007) 884-896
Reynolds A., Anderson E.M., Vermeulen A., Fedorov Y., Robinson K., Leake D., et al. Induction of the interferon response by siRNA is cell type- and duplex length-dependent. RNA 12 (2006) 988-993
Bonetta L. RNAi: silencing never sounded better. Nat Methods 1 (2004) 79-86
Haasnoot J., Westerhout E.M., and Berkhout B. RNA interference against viruses: strike and counterstrike. Nat Biotechnol 25 (2007) 1435-1443
Popescu F.D. Antisense- and RNA interference-based therapeutic strategies in allergy. J Cell Mol Med 9 (2005) 840-853
Elbashir S.M., Harborth J., Weber K., and Tuschl T. Analysis of gene function in somatic mammalian cells using small interfering RNAs. Methods 26 (2002) 199-213
Reynolds A., Leake D., Boese Q., Scaringe S., Marshall W.S., and Khvorova A. Rational siRNA design for RNA interference. Nat Biotechnol 22 (2004) 326-330
Pei Y., and Tuschl T. On the art of identifying effective and specific siRNAs. Nat Methods 3 (2006) 670-676
Lu P.Y., Xie F., and Woodle M.C. In vivo application of RNA interference: from functional genomics to therapeutics. Adv Genet 54 (2005) 117-142
Omi K., Tokunaga K., and Hohjoh H. Long-lasting RNAi activity in mammalian neurons. FEBS Lett 558 (2004) 89-95
Corey D.R. Chemical modification: the key to clinical application of RNA interference?. J Clin Invest 117 (2007) 3615-3622
De Paula D., Bentley M.V., and Mahato R.I. Hydrophobization and bioconjugation for enhanced siRNA delivery and targeting. RNA 13 (2007) 431-456
Aigner A. Gene silencing through RNA interference (RNAi) in vivo: strategies based on the direct application of siRNAs. J Biotechnol 124 (2006) 12-25
Bumcrot D., Manoharan M., Koteliansky V., and Sah D.W. RNAi therapeutics: a potential new class of pharmaceutical drugs. Nat Chem Biol 2 (2006) 711-719
McNamara II J.O., Andrechek E.R., Wang Y., Viles K.D., Rempel R.E., Gilboa E., et al. Cell type-specific delivery of siRNAs with aptamer-siRNA chimeras. Nat Biotechnol 24 (2006) 1005-1015
Oliveira S., Storm G., and Schiffelers R.M. Targeted Delivery of siRNA. J Biomed Biotechnol 2006 (2006) 63675
Wiewrodt R., Thomas A.P., Cipelletti L., Christofidou-Solomidou M., Weitz D.A., Feinstein S.I., et al. Size-dependent intracellular immunotargeting of therapeutic cargoes into endothelial cells. Blood 99 (2002) 912-922
Muro S., Wiewrodt R., Thomas A., Koniaris L., Albelda S.M., Muzykantov V.R., et al. A novel endocytic pathway induced by clustering endothelial ICAM-1 or PECAM-1. J Cell Sci 116 (2003) 1599-1609
Stahl P.D., and Ezekowitz R.A. The mannose receptor is a pattern recognition receptor involved in host defense. Curr Opin Immunol 10 (1998) 50-55
Engering A.J., Cella M., Fluitsma D., Brockhaus M., Hoefsmit E.C., Lanzavecchia A., et al. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur J Immunol 27 (1997) 2417-2425
DesJardin L.E., Kaufman T.M., Potts B., Kutzbach B., Yi H., and Schlesinger L.S. Mycobacterium tuberculosis-infected human macrophages exhibit enhanced cellular adhesion with increased expression of LFA-1 and ICAM-1 and reduced expression and/or function of complement receptors, FcgammaRII and the mannose receptor. Microbiology 148 (2002) 3161-3171
Kanters D., ten Hove W., Luijk B., van Aalst C., Schweizer R.C., Lammers J.W., et al. Expression of activated Fc gamma RII discriminates between multiple granulocyte-priming phenotypes in peripheral blood of allergic asthmatic subjects. J Allergy Clin Immunol 120 (2007) 1073-1081
Park S.G., Choi J.W., Kim H., Roh G.S., Bok J., Go M.J., et al. Genome-wide profiling of antigen-induced time course expression using murine models for acute and chronic asthma. Int Arch Allergy Immunol 146 (2008) 44-56
Acuff H.B., Sinnamon M., Fingleton B., Boone B., Levy S.E., Chen X., et al. Analysis of host- and tumor-derived proteinases using a custom dual species microarray reveals a protective role for stromal matrix metalloproteinase-12 in non-small cell lung cancer. Cancer Res 66 (2006) 7968-7975
McIntyre G.J., and Fanning G.C. Design and cloning strategies for constructing shRNA expression vectors. BMC Biotechnol 6 (2006) 1
Nakao I., Kanaji S., Ohta S., Matsushita H., Arima K., Yuyama N., et al. Identification of pendrin as a common mediator for mucus production in bronchial asthma and chronic obstructive pulmonary disease. J Immunol 180 (2008) 6262-6269
Buning H., Perabo L., Coutelle O., Quadt-Humme S., and Hallek M. Recent developments in adeno-associated virus vector technology. J Gene Med 10 (2008) 717-733
Boeckle S., and Wagner E. Optimizing targeted gene delivery: chemical modification of viral vectors and synthesis of artificial virus vector systems. AAPS J 8 (2006) E731-E742
Gipps E.M., Arshady R., Kreuter J., Groscurth P., and Speiser P.P. Distribution of polyhexyl cyanoacrylate nanoparticles in nude mice bearing human osteosarcoma. J Pharm Sci 75 (1986) 256-258
Bosquillon C., Lombry C., Preat V., and Vanbever R. Influence of formulation excipients and physical characteristics of inhalation dry powders on their aerosolization performance. J Control Release 70 (2001) 329-339
Azarmi S., Roa W.H., and Lobenberg R. Targeted delivery of nanoparticles for the treatment of lung diseases. Adv Drug Deliv Rev 60 (2008) 863-875
Li B.J., Tang Q., Cheng D., Qin C., Xie F.Y., Wei Q., et al. Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque. Nat Med 11 (2005) 944-951
Huang H.Y., Lee C.C., and Chiang B.L. Small interfering RNA against interleukin-5 decreases airway eosinophilia and hyper-responsiveness. Gene Ther 15 (2008) 660-667
Lee C.C., Huang H.Y., and Chiang B.L. Lentiviral-mediated GATA-3 RNAi decreases allergic airway inflammation and hyperresponsiveness. Mol Ther 16 (2008) 60-65
Durcan N., Murphy C., and Cryan S.A. Inhalable siRNA: potential as a therapeutic agent in the lungs. Mol Pharm 5 (2008) 559-566
Deroanne C., Vouret-Craviari V., Wang B., and Pouyssegur J. EphrinA1 inactivates integrin-mediated vascular smooth muscle cell spreading via the Rac/PAK pathway. J Cell Sci 116 (2003) 1367-1376
Persengiev S.P., Zhu X., and Green M.R. Nonspecific, concentration-dependent stimulation and repression of mammalian gene expression by small interfering RNAs (siRNAs). RNA 10 (2004) 12-18
Judge A., and MacLachlan I. Overcoming the innate immune response to small interfering RNA. Hum Gene Ther 19 (2008) 111-124
Zamanian-Daryoush M., Marques J.T., Gantier M.P., Behlke M.A., John M., Rayman P., et al. Determinants of cytokine induction by small interfering RNA in human peripheral blood mononuclear cells. J Interferon Cytokine Res 28 (2008) 221-233
Sioud M. Does the understanding of immune activation by RNA predict the design of safe siRNAs?. Front Biosci 13 (2008) 4379-4392
Yang M., Huang H., Li J., Huang W., and Wang H. Connective tissue growth factor increases matrix metalloproteinase-2 and suppresses tissue inhibitor of matrix metalloproteinase-2 production by cultured renal interstitial fibroblasts. Wound Repair Regen 15 (2007) 817-824
Emi N., Friedmann T., and Yee J.K. Pseudotype formation of murine leukemia virus with the G protein of vesicular stomatitis virus. J Virol 65 (1991) 1202-1207
Sirven A., Pflumio F., Zennou V., Titeux M., Vainchenker W., Coulombel L., et al. The human immunodeficiency virus type-1 central DNA flap is a crucial determinant for lentiviral vector nuclear import and gene transduction of human hematopoietic stem cells. Blood 96 (2000) 4103-4110
